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Climate and Environmental Change in the Mediterranean
Basin – Current Situation and Risks for the Future First
Mediterranean Assessment Report (MAR1)
Chapter 4 Ecosystems Coordinating Lead Authors: Mario V. Balzan
(Malta), Abed El Rahman Hassoun (Lebanon)
Lead Authors: Najet Aroua (Algeria), Virginie Baldy (France),
Magda Bou Dagher (Lebanon), Cristina Branquinho (Portugal),
Jean-Claude Dutay (France), Monia El Bour (Tunisia), Frédéric
Médail (France), Meryem Mojtahid (Morocco/France), Alejandra
Morán-Ordóñez (Spain), Pier Paolo Roggero (Italy), Sergio Rossi
Heras (Italy), Bertrand Schatz (France), Ioannis N. Vogiatzakis
(Cyprus), George N. Zaimes (Greece), Patrizia Ziveri (Spain)
Contributing Authors:
Marie Abboud-Abi Saab (Lebanon), Aitor Ameztegui (Spain),
Margaretha Breil (Italy), Thierry Gauquelin (France), llse R.
Geijzendorffer (France), Aristeidis Koutroulis (Greece), Jürg
Luterbacher (Germany), Moham-mad Merheb (Lebanon), Cesar Terrer
Moreno (Spain), Marco Turco (Spain), Elena Xoplaki (Germany)
This chapter should be cited as: Balzan MV, Hassoun AER, Aroua
N, Baldy V, Bou Dagher M, Branquinho C, Du-tay J-C, El Bour M,
Médail F, Mojtahid M, Morán-Ordóñez A, Roggero PP, Rossi Heras S,
Schatz B, Vogiatzakis IN, Zaimes GN, Ziveri P 2020 Ecosystems. In:
Climate and Environmental Change in the Mediterranean Basin –
Current Situation and Risks for the Future. First Mediterranean
Assessment Report [Cramer W, Guiot J, Marini K (eds.)] Union for
the Mediterranean, Plan Bleu, UNEP/MAP, Marseille, France, 151pp,
in press
(Final text before page editing for print)
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Table of Contents 4 Ecosystems
............................................................................................................................
5
Executive summary
.........................................................................................................................
5 4.1 Marine ecosystems
....................................................................................................................
6
4.1.1 Current condition and past trends
....................................................................................................
6 4.1.1.1 Observed changes
.....................................................................................................................
6
Key habitats undergoing change
.......................................................................................................
8 Coralligenous
................................................................................................................................
8 Deep sea ecosystems
..................................................................................................................
10 Planktonic ecosystems
................................................................................................................
10 Large vertebrates
........................................................................................................................
12
Changes in biodiversity
...................................................................................................................
14 4.1.1.2 Past changes
............................................................................................................................
17
Response of marine ecosystems to past temperature changes
..................................................... 17 Response
of marine ecosystems to past changes in stratification and
ventilation ........................ 18 Response of marine
ecosystems to past changes in productivity
................................................... 18 Response of
marine ecosystems to past changes in pH
..................................................................
19
4.1.2 Projected vulnerabilities and risks
..................................................................................................
19 4.1.2.1 Projected impacts and risks
.....................................................................................................
19
Projected impacts on microbes
.......................................................................................................
20 Projected impacts on primary and secondary production
.............................................................. 20
Projected impacts on macrobenthic and pelagic species
...............................................................
22
Corals
..........................................................................................................................................
22 Seagrass
......................................................................................................................................
23 Mussels
.......................................................................................................................................
24 Jellyfish
........................................................................................................................................
24
Winners and losers
..........................................................................................................................
24 4.1.2.2 Vulnerabilities
..........................................................................................................................
25
Climate-related vulnerabilities
........................................................................................................
25 Anthropogenic vulnerabilities
.........................................................................................................
26
4.1.3 Adaptation
......................................................................................................................................
26 4.1.3.1 Long-term monitoring and adaptation strategies
...................................................................
26 4.1.3.2 The role of Marine Protected Areas (MPAs) for adaptation
................................................... 27 4.1.3.3
Management of fisheries and adaptation
...............................................................................
28 4.1.3.4 Adaptation strategies for ocean warming and ocean
acidification in the Mediterranean Sea 29 4.1.3.5 Regional
observation networks as a tool for adaptation
........................................................ 30
4.2 Coastal ecosystems
.................................................................................................................
31 4.2.1 Current condition and past trends
..................................................................................................
31
4.2.1.1 Observed changes
...................................................................................................................
31 Natural Mediterranean habitats under severe degradation
........................................................... 31
Sandy beaches and sand dunes
..................................................................................................
32 Rocky coasts
................................................................................................................................
33 Coastal wetlands
.........................................................................................................................
34 Seagrass meadows
......................................................................................................................
34 Coastal lagoons and deltas
.........................................................................................................
35 Salt marshes
................................................................................................................................
36 Coastal aquifers
..........................................................................................................................
37
Risks from non-indigenous species
.................................................................................................
37 Phytoplankton
.............................................................................................................................
37 Jellyfish
........................................................................................................................................
38 Fish
..............................................................................................................................................
38 Plants
..........................................................................................................................................
39 Other non-indigenous species
....................................................................................................
39
4.2.1.2 Past changes
............................................................................................................................
40 Response of coastal ecosystems to past changes in sea level
........................................................ 40
Response of coastal ecosystems to past climate variability
............................................................ 41
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4.2.2 Projected vulnerabilities and risks
..................................................................................................
42 4.2.2.1 Projections and risks based on biological groups
....................................................................
42
Phytoplankton
.................................................................................................................................
42 Fish
..................................................................................................................................................
43 Seaweed
..........................................................................................................................................
44 Corals
...............................................................................................................................................
44
4.2.2.2 Projections and risks based on key natural habitats
............................................................... 45
Sandy beaches/dunes
.....................................................................................................................
45 Rocky shores
....................................................................................................................................
46 Coastal wetlands
.............................................................................................................................
46 Seagrass meadows
..........................................................................................................................
47 Coastal lagoons
...............................................................................................................................
47
Deltas...............................................................................................................................................
48 Coastal aquifers
...............................................................................................................................
49
4.2.2.3 Vulnerabilities
..........................................................................................................................
50 Coastal urbanization
........................................................................................................................
50 Sea level rise
....................................................................................................................................
52
4.2.3 Adaptation
......................................................................................................................................
52 4.2.3.1 Adaptation of different coastal systems
..................................................................................
52 4.2.3.2 Harmful algal bloom monitoring
.............................................................................................
53 4.2.3.3 Early detection of potentially dangerous species
....................................................................
54 4.2.3.4 Adaptation management strategies for the jellyfish
Pelagia noctiluca ................................... 54 4.2.3.5
Ecosystem-based adaptation management
............................................................................
55 4.2.3.6 The role of institutions/actors and local communities:
recommendations ............................ 56
4.3 Terrestrial and freshwater ecosystems
...................................................................................
56 4.3.1 Current conditions and past trends
................................................................................................
56
4.3.1.1 Past climate variability and its impact on terrestrial
ecosystems ........................................... 56 4.3.1.2
Direct human impacts on ecosystems in the past
...................................................................
57
Forests
.............................................................................................................................................
59 The human footprint in Mediterranean forests
.........................................................................
60 Ecosystem services provision by Mediterranean forests
............................................................ 61
Mountains
.......................................................................................................................................
62 Land use changes in mountain regions
.......................................................................................
63 Mountain biodiversity changes
...................................................................................................
63
Drylands and shrublands
.................................................................................................................
64 Agroecosystems
..............................................................................................................................
66
Agroecosystem development in different regions
.....................................................................
66 Grasslands and grazing
systems..................................................................................................
70 Ecosystem services related to pollination
..................................................................................
70
Freshwater ecosystems
...................................................................................................................
71 River regulation
...........................................................................................................................
71 Groundwater depletion
..............................................................................................................
72 Hydrologic regimes
.....................................................................................................................
72 Land-use changes, reduction of wetlands and riparian areas
.................................................... 73 Water
quality
..............................................................................................................................
74 Freshwater species
.....................................................................................................................
74 Protected areas (Natura 2000 network and Ramsar
Convention).............................................. 75
4.3.2 Projected vulnerabilities and risks
..................................................................................................
75 4.3.2.1 Forests
.....................................................................................................................................
75
Changes in forest ecosystem health and ecosystem services
provision ......................................... 76 Changes in
species range, abundance and extinction
.....................................................................
78 Fire activity and burnt areas across the Mediterranean
.................................................................
79
4.3.2.2 Mountains
................................................................................................................................
79 4.3.2.3 Drylands and shrublands
.........................................................................................................
80
Droughts
..........................................................................................................................................
82 4.3.2.4 Agriculture and pasturelands
..................................................................................................
82
Cropping systems
............................................................................................................................
84
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Grasslands and grazing systems
......................................................................................................
85 4.3.2.5 Freshwater ecosystems
...........................................................................................................
86
Rivers and streams
..........................................................................................................................
86 Wetlands
.........................................................................................................................................
87 Freshwater biodiversity
...................................................................................................................
87
4.3.3 Adaptation
......................................................................................................................................
87 4.3.3.1 Forests
.....................................................................................................................................
88
Biological adaptation
.......................................................................................................................
88 Limits to adaptation
........................................................................................................................
89 Measures to promote adaptation
...................................................................................................
90
4.3.3.2 Mountain ecosystems
..............................................................................................................
92 4.3.3.3 Drylands and shrublands
.........................................................................................................
92 4.3.3.4 Agriculture and pasturelands
..................................................................................................
93 4.3.3.5 Freshwater ecosystems
...........................................................................................................
96
Box 4.1: Bio-indicators for the assessment of changes in
Mediterranean marine ecosystems ... 99 Box 4.2: Urban biodiversity
in the Mediterranean Region
......................................................... 100
Consequences for biodiversity and ecosystem services in urban
areas ................................................ 100 Urban
biodiversity and ecosystem services
...........................................................................................
101
Box 4.3: Nitrogen deposition and ecosystems
............................................................................
102 Box 4.4: Mediterranean islands
...................................................................................................
102
Islands as laboratories
...........................................................................................................................
102 Recent evidence of change
....................................................................................................................
103 Climate change projections and islands
.................................................................................................
103 Vulnerability/resilience
..........................................................................................................................
104 Conservation and
adaptation.................................................................................................................
104
References
...................................................................................................................................
104
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4 Ecosystems
Executive summary Marine ecosystems
Despite covering only 0.82% of the ocean’s surface, the
Mediterranean Sea supports up to 18% of all known marine species,
with 21% being listed as vulnerable and 11% as endangered. The
accelerated spread of tropical non-indigenous species is leading to
the “tropicalization” of Mediterranean fauna and flora as a result
of warming and extreme heat waves since the 1990s. The
acidification rate in the Mediterranean waters has ranged between
0.055 and 0.156 pH units since the pre-industrial period, affecting
the marine trophic chain, from its primary pro-ducers (i.e.,
coccolithophores and foraminifera) to corals and coralline red
algae.
Projections for high emission scenarios show that endemic
assemblages will be modified with numerous species becoming extinct
in the mid 21st century and changes to the natural habitats of
commercially valuable species, which would have many repercussions
on marine ecosystem services such as tourism, fisheries, climate
regulation, and ultimately on human health.
Adaptation strategies to reduce environmental change impacts
need effective mitigation pol-icies and actions. They require
anticipatory planning to enable them to tackle problems while they
are still manageable. Given the diversity of each Mediterranean
sub-basin, wider moni-toring coverage is needed to strengthen our
knowledge about the different adaptation pro-cesses that
characterize and best suit each geographical zone. Adaptation
implies the imple-mentation of more sustainable fishing practices
as well as reducing pollution from agricultural activity,
sustainable tourism or developing more effective waste management.
Marine pro-tected areas can potentially have an insurance role if
they are established in locations not par-ticularly vulnerable to
ocean acidification and climate change.
Coastal ecosystems
The coastal zone, i.e. the area in which the interaction between
marine systems and the land dominate ecological and resource
systems, is a hotspot of risks, especially in the south-eastern
Mediterranean region. Alterations to coastal ecosystems (lagoons,
deltas, salt marshes, etc.) due to climate change and human
activities affect the flow of nutrients to the sea, the magni-tude,
timing and composition of potentially harmful/toxic plankton
blooms. They also signifi-cantly increase the number and frequency
of jellyfish outbreaks, and could have negative im-pacts on
fisheries. 1.2 to 5% of seagrass meadows in the Mediterranean Sea,
which represent 5 to 17% of the worldwide seagrass habitat, are
lost each year. Among them, almost half of the surveyed Posidonia
oceanica sites have suffered net density losses of over 20% in 10
years. As for fish, non-indigenous species and climate change cause
local extinction.
Projected temperature increases combined with a decrease in
nutrient replenishment and ocean acidification, are expected to
cause changes in plankton communities, negative impacts on fish,
corals, seagrass meadows and propagation of non-indigenous species.
Projected sea level rise will impact coastal wetlands deltas and
lagoons. Extensive urbanization added to cli-mate change is also
expected to threaten coastal ecosystems, human health and
well-being.
A nexus approach is required when trying to establish adaptation
methods for the entire Med-iterranean, while taking into account
ecosystem-based management, synergies and conflicts, integrating
local knowledge and institutions. Suitable adaptation policies
include reducing pol-lution runoff, both from agriculture and
industry and waste management, and policies to limit or prevent
acidification. Conservation planning and management should focus on
cross-cutting approaches and building resilience between structural
and functional connectivities of various fields.
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Terrestrial ecosystems
Biodiversity changes in the Mediterranean over the past 40 years
have occurred more quickly and been more significant than in other
regions of the world. Urbanization and the loss of grasslands are
key factors of ecosystem degradation across the region. Since 1990,
agricultural abandonment has led to a general increase in forest
areas in the northern Mediterranean, while in the southern
Mediterranean, ecosystems are still at risk of fragmentation or
disap-pearance due to human pressure from clearing and cultivation,
overexploitation of firewood and overgrazing. Drylands have
significant biodiversity value, with many of the plants and
an-imals highly adapted to water-limited conditions. They are
undergoing an overall increase in response to climate change and
extensive land abandonment. 48% of Mediterranean wetlands were lost
between 1970 and 2013, with 36% of wetland-dependent animals in the
Mediterra-nean threatened with extinction. Because of the reduction
in river flows, 40% of fish species in Mediterranean rivers are
endangered.
Projections for the 21st century indicate drier climate and
increased human pressure, with neg-ative impacts on terrestrial
biodiversity, forest productivity, burned areas, freshwater
ecosys-tems and agrosystems. Future projections indicate that burnt
areas can increase across the region by up to 40% in a 1.5°C
warming scenario and up to 100% from current levels for 3°C warming
at the end of the century. Mediterranean drylands will become drier
and their extent is expected to increase across the region.
Projections suggest decreased hydrological connec-tivity, increased
concentration of pollutants during droughts, changes in biological
communi-ties as a result of harsher environmental conditions, and a
decrease in biological processes such as nutrient uptake, primary
production, and decomposition.
Promotion of ‘climate-wise connectivity’ through permeability of
the landscape matrix, disper-sal corridors and habitat networks are
key to facilitating upward the migration of lowland spe-cies to
mountains in order to adapt to new climate change conditions.
Promotion of mixed-species forest stands and sylvicultural
practices such as thinning, and management of under-story can
promote the adaption of Mediterranean forests to climate change.
Promotion of the spatial heterogeneity of the landscape matrix can
help reduce fire impacts. The preservation of the natural flow
variability of Mediterranean rivers and streams and wide riparian
areas, along with reductions in water demand are key to the
adaptation of freshwater ecosystems to future climate change.
4.1 Marine ecosystems
4.1.1 Current condition and past trends
4.1.1.1 Observed changes
Despite only covering 0.82% of the ocean surface, the
Mediterranean Sea supports a high level of bio-diversity, including
about 18% of all known marine species (~ 17,000) (Bianchi and Morri
2000; UNEP/MAP-RAC/SPA 2009; Coll et al. 2010). The Mediterranean
Sea is biologically diverse because it is a warm sea at temperate
latitudes, and is thus home to both temperate and subtropical
species, and has been further diversified by its complex geological
history (Bianchi and Morri 2000; Merheb et al. 2016). As a result,
the present marine biota of the Mediterranean is composed of
species belonging to: (1) temperate Atlantic-Mediterranean species;
(2) cosmopolitan species; (3) endemic elements, comprising both
paleoendemic (Tethyan origin) and neoendemic species (Pliocenic
origin); (4) sub-tropical Atlantic species (interglacial remnants);
(5) boreal Atlantic species (ice-age remnants); (6) Red Sea
migrants (especially into the Levantine basin); (7) eastern
Atlantic migrants (especially into the Alboran Sea) (Bianchi and
Morri 2000).
In marine ecosystems, specific drivers of environmental change
include: i) the increasing temperature and salinity of surface
waters (Coma et al. 2009; Conversi et al. 2010; Calvo et al. 2011)
and the deep-
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sea (≥400 m) (Béthoux et al. 1990; Rixen et al. 2005;
Vargas-Yáñez et al. 2010; Skliris et al. 2014; Schroeder et al.
2016), ii) enhanced thermal stratification (Powley et al. 2016),
which can increase eutrophication and O2 consumption due to
increasing dissolved organic carbon (DOC) concentrations in the
mixed layer (Ferreira et al. 2011; Santinelli et al. 2013; Ngatia
et al. 2019), and iii) decreasing ocean pH fundamentally changing
ocean carbonate chemistry (Calvo et al. 2011; The MerMex Group et
al. 2011; Flecha et al. 2015; Hassoun et al. 2015, 2019; Merlivat
et al. 2018). Detailed information about these drivers, namely
temperature and salinity changes, Mediterranean hydrology and ocean
acidification can be found in Sections 2.2.4, 2.2.7.2 and 2.2.9.
Risks and vulnerabilities caused by these drivers are also affected
by non-climate related anthropogenic stressors, such as
industrialization, ur-banization and agriculture, fishing, maritime
traffic, harbor activities, tourism (Macías et al. 2014; Thiébault
et al. 2016) and floating plastics and other polymers (Fossi et al.
2012, 2018; Suaria et al. 2016). These non-climate drivers are
thoroughly described in Chapters 2 and 3.1 (Section 3.1.2.3) and
can be classified as pollution (Section 2.3) and land and sea-use
changes (Section 2.4).
The interconnected effects of climate change and several
non-climate related drivers, covered in Chap-ter 2, Section 2.6
affect the way the Mediterranean marine ecosystem functions at all
levels, from primary producers to upper trophic-levels (The MerMex
Group et al. 2011; Doney et al. 2012; IPCC 2014) (Figure 4.1).
Consequences include enhanced mortality of key marine habitat
species, e.g., cor-alligenous outcrops, maërl beds (Pairaud et al.
2014; Molina et al. 2016) and the bivalve Pinna nobilis
(Vázquez-Luis et al. 2017), as well as the increased establishment
of new communities and disease outbreaks (Rubio-Portillo et al.
2018; Berzak et al. 2019). Impacts of warming on marine biota not
only result from the direct impact of increasing temperature on
organism physiology, but also from the effect of warming on other
biological (e.g., microbial activity, metabolic rates) and abiotic
(e.g., oxygen solubility) components of ecosystem functions
(Vaquer-Sunyer and Duarte 2013).
Since the mid-1980s, regime shifts in the Mediterranean Sea have
impacted different ecosystem com-ponents (e.g., diversity and
abundance of zooplankton, abundance of anchovy stocks, frequency of
harmful algal blooms, mucilage outbreaks), possibly due to regional
effects of climate modes (Section 2.2.2), such as a positive state
of the North Atlantic Oscillation (NAO) that affects the physical
proper-ties of the water column (Conversi et al. 2010; Barausse et
al. 2011). The recent study by Fortibuoni et al. (2017), while
confirming the existence of some regime shifts, does not support
the hypothesis of climatic change as a main driver for these, and
rather points to the impact of local pressures, i.e.
over-exploitation and nutrient loads.
Increasing temperatures are driving the northward spread of
warm-water species (Sabatés et al. 2006; Tsikliras 2008; Bianchi et
al. 2018), and have contributed to the spread of the non-indigenous
Atlantic coral Oculina patagonia (Serrano et al. 2013). The recent
spread of warm-water species that have en-tered from Red Sea and
Atlantic Ocean into cooler northern areas is leading to the
“tropicalization” of Mediterranean fauna (Vergés et al. 2014;
Bianchi et al. 2018; Galil et al. 2018). Non-indigenous species are
extensively detailed as a driver in Section 2.5. Species that need
certain temperature ranges cannot migrate further, as the different
areas in which they usually live and span are becoming more and
more restricted, e.g., the anchovy Engraulis engrasicolus (Sabatés
et al. 2006). Warming water may also have strong effects on deep
Mediterranean areas of the two zones were cold water is formed, as
increasing temperature may slow the potential downwelling and the
provision of oxygen both in the Gulf of Lions and in the Adriatic
Sea, leaving the cold-water coral communities exposed to a certain
degree of hy-poxia (Taviani et al. 2016).
In addition to the general warming patterns, periods of extreme
temperatures have had large-scale and negative consequences for
Mediterranean marine ecosystems (Sections 2.2.1 and 2.2.2). A link
between positive thermal anomalies and observed invertebrate mass
mortalities has been observed in the Mediterranean Sea (Rivetti et
al. 2014). Also, unprecedented mass mortality events, which
af-fected at least 25 prominent sessile metazoans, occurred during
the summers of 1999, 2003, and 2006 across hundreds of kilometers
of coastline in the northwest Mediterranean Sea (Cerrano et al.
2000; Calvo et al. 2011). These events coincided with either short
periods (2 to 5 days: 2003, 2006) of high
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sea temperatures (27°C) or longer periods (30 to 40 days) of
less extreme temperatures (24°C: 1999) (Crisci et al. 2011).
Impacts of these events on marine organisms have particularly been
reported be-tween 0 and 35 m depths, such as gorgonian coral
mortality (Coma et al. 2009) or shoot mortality and flowering of
seagrasses (Díaz-Almela et al. 2007; Marba and Duarte 2010). A
collaborative database for tracking mass mortality events in the
Mediterranean Sea has been recently launched to support the
analysis of relationships between thermal conditions and/or other
environmental drivers (Garra-bou et al. 2019), and can be helpful
for better detecting changes across the Mediterranean Basin.
In addition, ocean acidification is an emerging human health
issue, that also threatens the marine realm (Falkenberg et al.
2020) (Section 2.2.9). Studies of the consequences of ocean
acidification on marine Mediterranean ecosystems report diverse
responses (Martin and Gattuso 2009; Rodolfo-Metalpa et al. 2010;
Movilla et al. 2012; Bramanti et al. 2013; Gazeau et al. 2014;
Lacoue-Labarthe et al. 2016). Insights have been gained by studying
natural CO2 seeps at Mediterranean sites such as Ischia and Vulcano
in Italy, where biodiversity decreases with decreasing pH toward
the vents, with a notable decline in calcifiers (Hall-Spencer et
al. 2008; Prada et al. 2017). Transplants of corals, mollusks, and
bryozoans along the acidification gradients around seeps reveal a
low level of vulnerability to CO2 lev-els expected over the next
100 years (Rodolfo-Metalpa et al. 2010, 2011). However, periods of
high temperature increase vulnerability to ocean acidification,
thereby increasing the long-term risk posed to Mediterranean
organisms and ecosystems as temperatures rise (Gazeau et al. 2014;
Lacoue-Lab-arthe et al. 2016). Ocean acidification seems to have a
slower but unstoppable effect on several or-ganisms, the increase
of temperature being a more immediate stress factor in most species
(Lejeusne et al. 2010). A recent overview (Gao et al. 2020) showed
that the combination of ocean acidification and warming may affect
food webs from different directions; ocean acidification is more
likely to fol-low bottom-up controls (resource driven), while
temperature drives top–down controls (consumer driven).
Key habitats undergoing change
Rapid warming of the Mediterranean Sea, in synergy with other
climate and non-climate related driv-ers (see Chapter 2), threatens
marine biodiversity, and particularly some key ecosystems that have
high vulnerability to such pressures, as presented below.
Coralligenous
The coralligenous is a typical Mediterranean underwater
seascape, present on hard bottoms from ~15 to 120 m depths and is
mainly produced by the accumulation of calcareous encrusting algae
(Litho-phyllum, Lithothamnion, Mesophyllum and Peyssonnelia)
growing in dim light conditions and relatively calm waters
(Ballesteros 2006; Boudouresque et al. 2015). These outcrops foster
one of the richest assemblages found in the Mediterranean,
harboring approximately 10% of Mediterranean marine spe-cies (Ros
et al. 1985; Boudouresque 2004; Ballesteros 2006; Casas-Güell et
al. 2016), most of which are long-lived algae and sessile
invertebrates (sponges, corals, bryozoans and tunicates) (Garrabou
et al. 2002; Ballesteros 2006). The different habitats that make up
these biogenic formations are mainly determined by light exposure,
so that some coralligenous habitats can be dominated by calcareous
algae and others completely dominated by macroinvertebrates with
almost no algae (Gili et al. 2014; Casas-Güell et al. 2016). Red
coral, Corallium rubrum, is one of the habitat-forming species that
plays a key role in the functioning of coralligenous habitats
because of its trophic activity, biomass and per-ennial biogenic
structure, like other Mediterranean gorgonian species (Gili et al.
2014; Ponti et al. 2014b, 2016, 2018). Red coral is a slow-growing,
long-lived species that grows in dim light habitats (e.g., caves,
vertical cliffs and overhangs) between 10 and 200 m depths. Despite
its essential ecosys-temic role, little is known about the
geographical distribution of red coral up to 400 km offshore the
coastline due to its large bathymetric range and afferent
constraints (Casas-Güell et al. 2015, 2016), and the major studies
focus on the phytobenthic component (Piazzi et al. 2009, 2012;
Boudouresque et al. 2015). Studies at an intermediate scale (tens
of km) have been conducted with key species, pin-pointing the fact
that their distribution may be very heterogeneous depending on the
environmental
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factors (Gori et al. 2012; Coppari et al. 2014, 2016). Due to
this lack of baseline data, the structure of coralligenous outcrops
is still poorly understood, preventing a proper assessment of its
current state of biodiversity and the potential impacts of
harvesting, and other disturbances related to global change, on red
coral assemblages. A recent study (Mallo et al. 2019) based on
historical red coral data from the north western Mediterranean Sea,
documented the halt in the C. rubrum decrease and the first
recovery response due to effective protection measures in some
areas.
Coralligenous outcrops are affected by several consequences of
global change such as nutrient enrich-ment, non-indigenous species,
increased sedimentation, mechanical impacts, mainly from fishing
ac-tivities, e.g., mechanical injuries and sediment re-suspension
(Cebrián et al. 2012; Piazzi et al. 2012; Gatti et al. 2015), as
well as sea warming (e.g., massive mortalities related to
temperature anomalies) and the potential effects of ocean
acidification (Bramanti et al. 2013; Cerrano et al. 2013; Gili et
al. 2014). Recently, potential synergies between these stressors
have been hypothesized (Section 2.6), especially in shallow areas
were heat waves may have a large impact on several organisms (Galli
et al. 2017), resulting in a fragmentation of the habitat that can
open new space for non-indigenous species (Vezzulli et al. 2013).
It has also been demonstrated that a decrease in the abundance of
coralligenous habitat-forming species leads to a rapid
fragmentation in community structure and a loss of species
benefiting from the structural complexity these species provide
(Ponti et al. 2014b; di Camillo and Cerrano 2015; Valls et al.
2015).
In addition to marine heat waves (Garrabou et al. 2001, 2009),
one of the main past threats for the red coral Corallium rubrum has
been intensive harvesting (see section 2.4), which has caused an
overall shift in population structure, resulting in a decrease in
both biomass and colony size (Tsounis et al. 2010; Bramanti et al.
2014; Montero-Serra et al. 2015). Moreover, its Mg-calcite skeleton
makes it vulnerable to ocean acidification (Bramanti et al. 2015).
Bramanti et al. (2013) experimentally evalu-ated the effects of low
pH on C. rubrum over a 314-day period under two pH levels (8.10 and
7.81). This study concludes that exposure to lower pH conditions
negatively affected skeletal growth and spicule morphology (i.e.,
abnormal shapes).
Mediterranean gorgonian “forests” (e.g., Paramuricea clavata,
Eunicella cavolinii) are threatened by several human activities and
are affected by climatic anomalies that have led to mass mortality
events in recent decades (Ponti et al. 2014b, 2018; Verdura et al.
2019). Observed mortality events have been linked to
temperature-dependent bacterial pathogens (Bally and Garrabou
2007). Also, diverse re-sponses to thermal stress have been shown
in gorgonians (Pivotto et al. 2015; Crisci et al. 2017). This may
condition the future response of these species to climate
change.
The ecological role of these habitats and the possible
consequence of their loss are still poorly under-stood. The
experimental study of Ponti et al. (2014b) reports a significant
effect of gorgonians (E. ca-volinii, and P. clavata) on the
recruitment of epibenthic organisms and their presence mainly
limits the growth of erect algae and enhances the abundance of
encrusting algae and sessile invertebrates. This effect could be
due to microscale modification of hydrodynamics and sediment
deposition rate by i) a shading effect that reduces light
intensity, ii) intercepting settling propagules, iii) competing for
food with filter-feeders and/or iv) competing for space by
producing allelochemicals. Although the biologi-cal interaction
between gorgonians and other species deserves further study,
changes to the edaphic conditions caused by gorgonian forests
influences the larval settlement and recruitment processes of
benthic assemblages (Ponti et al. 2014b, 2018).
In addition to the long-term effects of global change and its
consequences on the Mediterranean cor-alligenous, short-term
extreme events may be even more devastating than heat waves.
Teixidó et al. (2013) show how an extreme storm event affected the
dynamics of benthic coralligenous outcrops in the northwestern
Mediterranean Sea using data acquired before (2006–2008) and after
the impact (2009–2010) of a major storm. The most exposed and
impacted site experienced a major shift imme-diately after the
storm and over the following year. This impact consists of changes
in the species rich-ness and diversity of benthic species such as
calcareous algae, sponges, anthozoans, bryozoans and
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10
tunicates. In this site, benthic species recorded a 22% to 58%
loss of cover on average, with those with fragile forms showing
cover losses up to 50 to 100%. Small patches survived after the
storm and began to grow slightly during the following year, and the
sheltered sites showed no significant changes in all the studied
parameters, indicating no variations due to the storm (Teixidó et
al. 2013).
Deep sea ecosystems
Although poorly known, deep seafloor ecosystems provide services
that are vitally important to the entire ocean and biosphere, and
play a particularly major role in climate change mitigation. For
in-stance, by storing a large amount of anthropogenic CO2 and by
absorbing heat accumulated from the greenhouse effect, the deep sea
Mediterranean waters and ecosystems capture large quantities of
carbon and, as such, slow down the warming of surface waters and
land (Luna et al. 2012; Palmiéri et al. 2015) (Sections 2.2.7 and
2.2.9). Rising atmospheric greenhouse gases are affecting water
column oxygenation, temperature, pH and food supply (Section 3.2),
with similar impacts on deep-sea ecosys-tems (Sweetman et al.
2017). As they are deprived of light, deep-sea ecosystems are
greatly dependent on surface primary production: “marine snow”
(Gambi et al. 2014). Surface water also oxygenates deep-sea
environments when they sink to form deep and intermediate water
masses. When surface water is warmer, it does not mix well with
deep water (Section 2.2.7).
In the Mediterranean, the deep sea covers about 79% of the
Mediterranean Basin, including habitats potentially able to deliver
multiple ecosystem services and numerous resources of high economic
value (Manea et al. 2020). Despite this fact, very few studies
address the response of deep-sea ecosystems to ongoing climate
change in this sea. In contrast with most oceans where the flux of
particulate or-ganic matter to the seafloor is likely to decline
significantly in response to climate change (Sweetman et al. 2017),
a study from the eastern Mediterranean shows that climate change
has caused an imme-diate accumulation of organic matter on the
deep-sea floor in recent decades (Danovaro et al. 2001). This led,
together with deep-sea warming, to alteration of carbon and
nitrogen cycles and has had negative effects on deep-sea bacteria
and benthic fauna (Danovaro et al. 2001, 2004). For instance, the
observed salinity and temperature changes in eastern Mediterranean
deep and bottom waters from 1987 to 1994 (Roether et al. 1996;
Theocharis et al. 2002) led to the uplift of these water masses by
several hundred meters, reaching shallower depths (100–150 m; i.e.
close to the euphotic zone) under the influence of cyclonic
circulation. This resulted in increased biological production and
there-fore enhanced flux of organic carbon to the deep sea, thereby
significantly and quickly changing the way deep-sea ecosystems
function (Psarra et al. 2000; Danovaro et al. 2001). The review of
Yasuhara and Danovaro (2016) on temperature impacts on deep-sea
Mediterranean biodiversity shows that mi-nor temperature shifts of
around 0.1°C or less are sufficient to cause significant changes in
biodiversity and the community structure of deep-sea nematode
assemblages.
Planktonic ecosystems
Several studies have addressed the possible impact of climate
change on marine phytoplankton diver-sity and distribution in the
Mediterranean Sea, highlighting highly contrasting regional
patterns (Du-arte et al. 2000; Goffart et al. 2002; Marty et al.
2002; Bosc et al. 2004; Ribera d’Alcalà et al. 2004; Marty and
Chiavérini 2010; Herrmann et al. 2014; Oviedo et al. 2015; D’Amario
et al. 2017). Some studies from the northwestern Mediterranean have
reported a positive trend in phytoplankton bio-mass in response to
the expansion of the summer stratification. This trend was
accompanied by an increase in picoplankton and nanoflagellates
(i.e. small-sized phytoplankton) and a decline in diatoms, which
are responsible for new production (Goffart et al. 2002; Marty et
al. 2002; Mena et al. 2019; Ramírez-Romero et al. 2020). However,
other studies report that the spring bloom in many Mediter-ranean
regions tends to occur earlier in the year, possibly in relation to
earlier water warming and high irradiance, in contrast with the
autumn bloom that tends to disappear because of a longer
stratifica-tion period (Bosc et al. 2004). Bosc et al. (2004) also
reveal significant interannual variations in biomass and primary
production, not only in the northwestern basin (e.g., the
exceptional bloom in spring 1999), but also, and more surprisingly,
in the oligotrophic waters of the eastern basin (e.g., the 9%
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11
decrease in primary production from 2000 to 2001). In this
latter basin, phytoplankton shifts seem to be concurrent with
rising winter precipitation and sea surface temperature (Mena et
al. 2019) (Section 2.2.4, 2.2.5 and 2.2.7).
In some Mediterranean settings, such as the central Ligurian
Sea, increased deep-water convection (as deep as 2000 m) has been
attributed to greater surface salinity causing increased nutrient
supply near the surface, and thus more primary production (Marty
and Chiavérini 2010). In contrast, in the pro-ductive northwestern
Mediterranean Sea, deep convection could significantly decrease
under the in-fluence of climate change (Herrmann et al. 2014),
impacting pelagic planktonic ecosystem, which are strongly
influenced by these hydrodynamics. The weakening of deep convection
and surface warming modifies the pelagic planktonic ecosystem and
associated carbon cycle indirectly only: the spring bloom occurs
one month earlier, and the bottom up control of phytoplankton
development and bac-teria growth by nitrogen and phosphorus
availability strengthens, and the microbial loop intensifies as the
small-sized plankton biomass increases (Herrmann et al. 2014). Net
carbon fixation and deep ex-port do not change significantly. In
the Tyrrhenian Sea, Ribera d’Alcalà et al. (2004) explain the
signifi-cant changes in the long-term patterns of rare copepod
species as a symptom of large-scale meteoro-logical phenomena of
the North Atlantic sector.
In the NW Mediterranean Sea, decadal climatic oscillations
linked to the NAO forcing of the precipita-tion regime led to an
increase in the upper salinity in the 1980s and in the late 1990s
and early 2000s (Chapter 2, Section 2.2.7). In saline years, the
annual abundance of zooplankton is higher than other-wise
(Fernández de Puelles and Molinero 2007). According to Molinero et
al. (2008), large-scale climate forcing has altered the local
environment and the pelagic food-web dynamics in the NW
Mediterra-nean Sea through changes in biological interactions,
competition and predation. The authors also sug-gest that warming,
the dominance of small phytoplankton and predation pressure by
jellyfish nega-tively affected copepod populations (recruitment,
life-history traits and physiological thresholds) in the early
1990s, whereas chaetognaths were surpassed by jellyplankton as the
most frequent copepod prey. A more recent study from the same
Ligurian time-series updated with ten more years (up to 2003)
revealed that the zooplankton, mainly copepods, recovered their
initial concentrations after 2000, suggesting a quasi-decadal cycle
(Coma et al. 2009). This illustrates the difficulty in identifying
long-term changes from decadal oscillation in short time-series in
plankton. However, surface salinity appears to be a common physical
indicator of changes in the pelagic ecosystem of the NW
Mediterra-nean Sea for jellyfish (Buecher et al. 1997), crustaceans
(García-Comas et al. 2011) and phytoplankton (Marty and Chiavérini
2010).
Gallisai et al. (2014) report that aerosol deposition from the
Sahara may explain 1 to 10% of seasonally detrended chlorophyll
variability in the nutrient-low Mediterranean with main effects in
spring over the eastern and central Mediterranean, corresponding to
dust events fueling needed nutrients for the planktonic community
(Ternon et al. 2011). The areas showing negative effects on
chlorophyll from dust deposition are regions under significant
influence from European aerosols. Anthropogenic aerosol deposition
of nitrate and phosphate largely influence primary production in
the northern Mediterra-nean Sea (Richon et al. 2018a, 2018b)
(Section 2.2.3). This response of chlorophyll dynamics to dust
deposition is important when knowing that future scenarios predict
increased aridity and shallowing of the mixed layer (Gallisai et
al. 2014) (Section 2.3.2).
From around the island of Lampedusa (central Mediterranean), the
multi-year evolution of biogenic dimethylsulfide (DMS) production
in the marine surface layer and the resulting methanesulfonate on
the atmosphere are mainly attributed to phytoplankton physiology
(Becagli et al. 2013). High phyto-plankton productivity can also be
the expression of stressed cells, especially during summer when
high irradiance and the shallow depth of the upper mixed layer
prevails. This therefore leads to higher me-thanesulfonate
concentrations in the atmosphere. These dynamics can be further
controlled by the North Atlantic Oscillation, and related oceanic
and atmospheric processes (Becagli et al. 2013).
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12
Large vertebrates
One of the biggest threats to large marine vertebrates is litter
debris, such as fishing gear or other large items (Galgani et al.
2014) (Figure 4.1). Regularly, in the Mediterranean Sea and
worldwide, large ver-tebrates such as sea birds (van Franeker et
al. 2011), cetaceans (de Stephanis et al. 2013; Notarbartolo di
Sciara 2014) and marine turtles (Lazar and Gračan 2011; Campani et
al. 2013; Camedda et al. 2014) accidentally swallow micro and
macro-plastic debris that is often found in their digestive tracts.
The plastic debris (Section 2.3.2.3) affects the marine biota of
the Mediterranean at macro, micro- and nano-levels.
Figure 4.1 | Summary of interactions between large marine
vertebrates and marine litter (Gal-gani et al. 2014). Fluxes of
litter in the life cycle and intensity of its effects on large
marine verte-brates, (a: entanglement; b: ingestion), depending on
various factors such as ingestion mecha-nisms (predation, active or
passive filter feeding), development stage (benthic or pelagic
phases for sea turtles), behavior and foraging strategy (feeding on
the sea floor, in the water column or on the surface, selectivity
according to color, shape etc., ecological plasticity in diet and
habitat), types of litter (micro/macro litter) and types of fishing
gear (nets, hooks and lines). The thicker arrows indicate key
processes. Although trophic transfer from one level to another has
been demonstrated in vitro for microplastics in plankton, it
remains controversial in situ, as most in-gested litter is excreted
in feces.
Sperm whales (Physeter macrocephalus) in the Mediterranean Sea,
which are believed to be fewer than 2500 mature individuals, are
endangered world-wide (Notarbartolo di Sciara 2014). A decline in
sperm whales in the Mediterranean has been observed over the last
half-century. In addition to inges-tion of solid debris, other
anthropogenic activities at sea are suspected to have caused the
decline of this species and continue to threaten its survival in
various ways: bycatch, collisions with vessels, de-bilitation by
chemical pollution, anthropogenic noise, disturbance from
irresponsible whale watching
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13
and most likely climate change, and prey depletion (Notarbartolo
di Sciara 2014). Regarding specifically ingested debris, ingestion
rates are as high as 31% in some marine mammal populations, and
sub-lethal effects could result in impacts at the population level
(Baulch and Perry 2014). Campani et al. (2013) and Camedda et al.
(2014) investigated the interaction between loggerhead sea turtles
(Caretta caretta) and marine litter in the northern Tyrrhenian Sea
and around Sardinia, respectively. In thirty-one C. caretta
individuals found stranded or accidentally bycaught in northern
Tyrrhenian Sea, marine debris, mainly plastics, were present in 71%
of specimens (Campani et al. 2013). In Sardinia, only 14% of the
121 monitored turtles had debris in their digestive tracts but
plastic was the main physical cat-egory (Fossi et al. 2013; Camedda
et al. 2014).
Sharks and rays are also seriously threatened by anthropogenic
pressures, mainly as a result of over-fishing (Dulvy et al. 2014)
(Figure 4.2), as described in Section 2.4.2 in the context of the
increasing sea use changes. Some sharks live in narrow climatic
ranges (Chin et al. 2010), putting them at risk in a climate change
hotspot such as the Mediterranean (Ben Rais Lasram et al. 2010).
Microplastic (0 occur when more rays are landed than sharks. The
peak catch of taxonomically-differentiated rays peaks at 289,353
tonnes in 2003. (C) The main shark and ray fishing nations are
gray-shaded according to their per-centage share of the total
average annual chondrichthyan landings reported to the FAO from
1999 to 2009. The relative share of shark and ray fin trade exports
to Hong Kong in 2010 are rep-resented by fin size. The
taxonomically-differentiated proportion excludes the ‘nei’ (not
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14
elsewhere included) and generic ‘sharks, rays, and chimaeras’
category (adapted from Dulvy et al. 2014).
Changes in biodiversity
To date, changes in Mediterranean marine biodiversity are
essentially driven by human activities (Man-nino et al. 2017), i.e.
pollution (Section 2.3), sea use changes (Section 2.4.2), the
introduction of non-indigenous species (Section 2.5), together with
climate change (Section 2.2) (Lejeusne et al. 2010; Ze-netos et al.
2012; Katsanevakis et al. 2013, 2014b). In general, the
Mediterranean Sea represents the highest proportion of threatened
marine habitats in Europe (32%, 15 habitats) with 21% being listed
as vulnerable and 11% as endangered (see review in Mannino et al.
2017). This threat includes several valuable and unique habitats
(e.g., seagrasses and coralligenous), supporting an extensive
repository of biodiversity (Gubbay et al. 2016).
The shallow depth (on average 1450 m) of the Mediterranean Sea
and the relatively fast deep-water turnover in comparison to the
open ocean, coupled with a high degree of endemism (about 20% of
Mediterranean marine species; Coll et al. (2010)) point to a
potential amplification of climate change impacts. These are
expected to cause earlier changes in biodiversity in comparison
with other seas, thus making this system a model for investigating
biodiversity response to direct and indirect effects of temperature
changes and other climate-related and non-related drivers (Chapter
2).
Species with low dispersal ability are particularly affected by
climate change, which may also lead to local extinctions, greatly
contributing to biodiversity loss (Mannino et al. 2017). Any change
in biodi-versity may affect ecosystem functioning, even in the case
of the establishment of a single species and may lead to important
consequences both for nature as well as for society. However, the
extreme richness of microclimates in the Mediterranean (ranging
from climate conditions similar to those of the Northern Sea in the
Adriatic to an almost tropical condition in the eastern basin)
makes prediction at large spatial scales difficult. Most effects of
climate change (or climate anomalies) on marine biodi-versity have
been so far identified at regional scales (Philippart et al.
2011).
During recent decades, Mediterranean marine communities have
shown significant changes in taxa composition and distribution. In
the western Mediterranean, climate change is influencing the
bound-aries of biogeographic regions and thus warm water marine
species are extending their ranges and colonizing new regions where
they were previously absent (Katsanevakis et al. 2014a). For
instance, mucilages have appeared more frequently (associated with
a malfunctioning of the microbial loop) in the Adriatic Sea, where
it was documented for the first time, and in several regions
beyond, in recent decades, concomitantly with a significant
increase in sea surface temperature (Danovaro et al. 2009).
Mucilage is not closely associated with the presence of eutrophic
conditions, as several mucilage out-breaks have been recently
observed in oligotrophic seas, such as the Aegean Sea (Danovaro et
al. 2009). The Ligurian Sea, one of the coldest areas of the
Mediterranean Sea, displays a low number of subtropical species and
a higher abundance of cold-temperate water species. However, the
recent warming of Ligurian seawater has favored the penetration of
warm-water species (e.g., Thalassoma pavo), which from 1985 onward,
established large and stable populations (Parravicini et al.
2015).
Temperature anomalies, even of short duration, can dramatically
change Mediterranean faunal diver-sity. The largest mass-mortality
event recorded in the Mediterranean Sea so far occurred in 1999
along the French and Italian coasts (Cerrano et al. 2000; Perez et
al. 2000; Garrabou et al. 2001). That year was characterized by a
summer with a positive thermal anomaly that extended the
thermocline down to a depth of 40 m (Romano et al. 2000) and
resulted in the extensive mortality of 28 epibenthic inver-tebrate
species (Figure 4.3) (Perez et al. 2000; Rivetti et al. 2014).
Among benthic organisms, sponges and gorgonians were most severely
affected (Cerrano et al. 2000; Perez et al. 2000; Romano et al.
2000; Garrabou et al. 2001; Rivetti et al. 2014). The shortage of
food over several weeks is a common phenomenon in the Mediterranean
Sea due to summer water stratification, but very long periods with
high temperatures may explain such mass mortalities (Rossi et al.
2017a).
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15
In the eastern Mediterranean, the rise of seawater temperatures
may also be partly responsible for the entrance of non-indigenous
species (Section 2.5), mostly from the tropical Indo-Pacific (Galil
2000; Por 2009; Zenetos et al. 2012; Rilov 2016). The increased
introduction and spread of non-indigenous species may be a
supplementary stress factor for native species already weakened by
climate varia-tions resulting in the dislocation of indigenous
species’ niches and possibly cascade effects on the food webs
(Rilov 2016; Corrales et al. 2018). Non-indigenous species are a
recognized threat to diversity and the abundance of native species
as well as a threat to the ecological stability of the infested
eco-systems. Despite the overall tendency towards ocean warming,
the eastern Mediterranean also expe-riences occasional climate
anomalies, for example between 1992 and 1994, when temperatures
dropped by about 0.4°C (Danovaro et al. 2001). This caused a
drastic decrease in nematode abundance and overall faunal diversity
(e.g., a roughly 50% decrease in nematode diversity, Danovaro et
al. 2004). After 1994, when the temperature gradually recovered,
biodiversity started to reverse to previous conditions but had not
recovered fully in 1998 (Danovaro et al. 2004).
Figure 4.3 | Temperature trends across the Mediterranean Basin.
Temperature trends at 0–10 m (a), 11–30 m (b), 31–50 m (c) depth
layers for the period 1945–2011 in July-November. Linear
regressions have been calculated on grids of 1° latitude by 1°
longitude and tested for statistical significance at the 90% level.
Significant increased/decreased temperature trends are reported as
colored cells, non-significant increased/decreased temperature
trends are reported as grey ar-eas. Dots show the locations of
documented mass mortalities for a depth layer, each color
repre-sents a single event. The asterisks in the legend of mass
mortalities (MM) events refer to the taxa affected: * stands for
sponges, ** for cnidarians, *** for bryozoans, **** for ascidians,
***** for bivalves (Rivetti et al. 2014).
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16
Sea warming may also have effects on the virulence of pathogens,
favoring the frequency of epidemi-ological events, as most
pathogens are temperature sensitive (Bally and Garrabou 2007;
Vezzulli et al. 2013). Mass mortalities of the gorgonian
Paramunicea clavata, scleractinian corals, zoanthids, and sponges
observed in 1999 in the Ligurian Sea were indeed promoted by a
temperature shift, in con-junction with the growth of opportunistic
pathogens (including some fungi) (Cerrano et al. 2000).
Increased surface temperatures and altered circulation and
precipitation regimes have been evoked to explain the increased
frequency of bottom water hypoxia or anoxia in coastal areas of the
northern Adriatic. These phenomena, often associated with mass
mortalities of fish and benthic fauna, alter food webs and might
have important cascade effects on biodiversity (Coll et al. 2010).
The Adriatic Sea can undergo dramatic change in the lower part of
its temperature ranges. In winter 2001, the Adriatic Sea
experienced a period of abnormally low surface temperatures (from
9°C to freezing) that led to mass mortalities of sardines
(Sardinella aurita) (Guidetti et al. 2002), with resulting
alteration of the food webs. The Adriatic basin is also the site
for deep-water formation, as a result of the bora winds associated
with decreased temperatures, but recent studies have reported the
shift of this water for-mation site towards the Aegean Sea by a
phenomenon known as eastern-Mediterranean Transient (EMT), related
mainly to climatic sea and atmosphere conditions (Hassoun et al.
2015). EMTs change the salinity distribution with surface water
freshening linked to enhanced deep-water production and in turn to
strengthened Mediterranean thermohaline circulation (Incarbona et
al. 2016). This phenom-enon can thus affect the marine biodiversity
not only in the Adriatic and Ionian Seas but much further, as
documented by Ouba et al. (2016), who have correlated the salinity
variations and increase in total zooplankton abundance in Lebanese
waters to the activation of the Aegean Sea as a major source of
dense water formation as part of an “eastern Mediterranean
Transient-like” event (see Section 2.2.7 for more details about
Mediterranean circulation changes).
In response to ocean acidification, calcifying organisms
(planktonic and benthic) such as corals, foram-inifera,
coccolithophores and coralline red algae, important contributors of
marine calcium carbonate production, may be greatly affected
(Langer et al. 2009; Moy et al. 2009; Bramanti et al. 2013; Cerrano
et al. 2013; Kroeker et al. 2013). Based on experiments, the impact
of ocean acidification on Mediter-ranean corals was examined and a
significant decrease in calcification rates in most tested species
was reported (Movilla et al. 2012, 2014). In the latter study,
there was a heterogeneous effect of low pH on the skeletal growth
rate of the organisms depending on their initial weight, suggesting
that those specimens with high calcification rates may be the most
susceptible to the negative effects of acidifi-cation. Also, a
significant effect on benthic foraminiferal communities of low-pH
seawaters around the island of Ischia (Italy) has been demonstrated
as a result of volcanic gas vents with significant changes in
distribution, diversity and nature of the fauna (Dias et al.
2010).
Coccolithophores, which are the primary calcifying phytoplankton
group, and especially the most abundant species, Emiliania huxleyi,
have shown a reduction of calcification at increased CO2
concen-trations for the majority of strains tested in culture
experiments (Meyer and Riebesell 2015). Meier et al. (2014)
analyzed in situ E. huxleyi coccolith weight from the NW
Mediterranean Sea in a 12-year sediment trap series, and surface
sediment and sediment core samples. Their findings clearly show a
continuous decrease in the average coccolith weight of E. huxleyi
from 1993 to 2005, reaching levels below pre-industrial (Holocene)
and industrial (20th century) values recorded in the sedimentary
rec-ord, as most likely a result of the changes in the surface
ocean carbonate system. Also, a drastic de-crease in production,
species diversity and anomalous calcification in coccolithophores
has been shown along a natural pH gradient caused by marine CO2
seeps off Vulcano Island (Italy) (Ziveri et al. 2014).
To conclude, (1) Mediterranean fauna is highly vulnerable to
human activities and climate change; (2) both structural and
functional biodiversity of continental margins are significantly
affected by very small temperature changes; and (3) the impact of
human activities and climate change on marine bio-diversity might
be non-reversible. Since there are close interactions between deep
and shallow
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17
systems, the vulnerability of deep-sea ecosystems to climate
change might also have important impli-cations on the biodiversity
and functioning of continental shelves.
The extent of changes caused by climate and non-climate drivers,
the responses of Mediterranean marine biota to these changes and
their local-regional consequences are yet to be investigated, as
slow but significant transformations that may modify the neritic,
pelagic, and benthic zones are still ongoing.
4.1.1.2 Past changes
Understanding the degree to which changes in Mediterranean
marine ecosystems point to a direc-tional trend driven by global
warming remains a challenge for marine ecology (Bertolino et al.
2017a). Reconstructing the temporal variability of Mediterranean
marine ecosystems on time scales longer than a few centuries beyond
the instrumental records, crossing relevant climate variations and
histor-ical periods, can be critical for interpreting these
changes.
Climate forcings of Mediterranean marine ecosystems over the
past thousand years have occurred on different time scales
(Abrantes et al. 2005; Hennekam et al. 2014; Xoplaki et al. 2018).
During the Hol-ocene, rapid warming and cooling events have
occurred which can, to some degree, provide analogues for the
projected changes for the coming centuries (Blois et al. 2013;
Benito-Garzón et al. 2014; Raji et al. 2015). In the Mediterranean,
these past climate changes impacted the marine physico-chemical
parameters of surface and deep waters (e.g., salinity, temperature,
oxygenation, pH) which in turn affected marine ecosystems (Frigola
et al. 2008; Schmiedl et al. 2010a; Mojtahid et al. 2015; Bertolino
et al. 2017b).
Response of marine ecosystems to past temperature changes
In the Mediterranean region, the most abundant Holocene
temperature proxy data, especially for the Common Era (the last
2000 years) are alkenone-derived records (Abrantes et al. 2012;
Jalali et al. 2016; Sicre et al. 2016). These studies document
natural long-term trends superimposed on a multidecadal variability
in response to external (e.g., solar) and internal forcings (e.g.,
NAO) which might explain some recently observed sea surface
temperature trends (Versteegh et al. 2007). These studies also
reveal a strong regional component. For example, a high resolution
study from the Gulf of Lion shows an overall sea surface
temperature cooling trend since the mid-holocene followed by a
rapid warming from ~1850 AD onwards that may parallel recent
climate change (Jalali et al. 2016). In contrast, south of Sicily
and in the eastern Levantine basin, sea surface temperature records
show progressive warm-ing since the early Holocene without a clear
signature of the recent anthropogenic change (Castañeda et al.
2010; Luterbacher et al. 2012; Jalali et al. 2017). The planktonic
ecosystem in the Siculo–Tunisian Strait responded to this
progressive warming of the sea surface temperature by increasing
the abun-dance of warm dinocyst species (Spiniferites mirabilis and
Impagidinium aculeatum) and planktonic foraminifera (Globorotalia
inflata and Globigerinoides ruber) (Rouis-Zargouni et al.
2010).
The Holocene was interrupted by at least four brief cooling
events at ~9.2 ka, ~8 ka, ~7 ka and ~2.2 ka cal. BP, which may be
correlated to climate events recorded elsewhere, including in
Greenland ice cores and in Atlantic Ocean sediments. Investigations
on cetacean bones from the Grotta dell’Uzzo in northwestern Sicily
(Italy) show that the rapid climate change around 8 ka coincided
with increased strandings in the Mediterranean Sea (Mannino et al.
2015). Also, the diversity of sponge species living in
coralligenous habitats from the Ionian and Ligurian was strongly
affected by Holocene warming ep-isodes with a significant loss of
their biodiversity in recent decades (Bertolino et al. 2017b,
2019).
In the eastern Mediterranean, multiproxy records derived from
sediments from the southeastern Le-vantine (Schilman et al. 2001b;
Mojtahid et al. 2015) and the Adriatic Sea (Piva et al. 2008)
reveal complex paleo-oceanographic changes during the late
Holocene, with pronounced anomalies during the Medieval Warm Period
(MWP) (ca. AD 1150) and the Little Ice Age (ca. AD 1730). These
tempera-ture anomalies were accompanied in the eastern Levantine
basin by a drastic change in planktonic
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foraminiferal successions indicating periods oscillating between
cold and warm surface waters in op-posite phase with the western
Mediterranean records (Mojtahid et al. 2015). This east–west
contrast in the climate signals has been confirmed by other proxy
data (Jalali et al. 2016, 2017).
These findings imply that long-term and short-term
climate-driven environmental changes, caused by global warming,
will likely impact the entire food chain from planktonic ecosystems
to large mammals (e.g., cetaceans) in the near future.
Response of marine ecosystems to past changes in stratification
and ventilation
Throughout the Pleistocene, the eastern Mediterranean
experienced numerous anoxic events rec-orded by the cyclical
deposition of organic-rich layers or sapropels (Rossignol-Strick et
al. 1982; Rohling 1994), the most recent being Sapropel S1 from ~10
to 6 cal ka BP. Maximum insolation due to the Earth’s orbital
precession minimum significantly intensified the northeast African
monsoon, leading to enhanced discharge of fresh and nutrient-rich
Nile River water into the eastern Mediterranean (Ros-signol-Strick
et al. 1982; Emeis et al. 2000). In the Levantine basin, sea
surface salinity during S1 dropped by about 2.0 to 4.0 units
compared to present values (Kallel et al. 1997; Myers et al. 1998).
This led to severe water column stratification and organic
enrichment from the Nile river water. In the Ionian Sea, the
correspondence of recent sapropel layers with peaks of the lower
photic zone cocco-lithophore species Florisphaera profunda
indicated the development of a deep chlorophyll maximum, due to the
pycnocline/nutricline shallowing in the lower part of the photic
zone (Incarbona et al. 2011). In the SE Levantine basin, a severe
drop in planktonic foraminiferal diversity was recorded in response
to the water column stratification and expressed by the near
exclusive presence of the euryhaline tropical-subtropical species
Globigerinoides ruber and the disappearance of deep-dwelling
species (Mojtahid et al. 2015).
The combination of higher organic matter remineralization and
decreased ventilation resulted in wide-spread bottom water anoxia
(Rohling 1994; Hennekam et al. 2014). In the Southern Aegean and
Le-vantine Seas, there was a gradual increase in deep-water
residence times, preceding S1 formation by approximately 1–1.5 kyr.
Once oxygen levels fell below a critical threshold, the benthic
ecosystems collapsed almost synchronously with the onset of S1
deposition. The recovery of benthic ecosystems during the terminal
phase of S1 formation is controlled by subsequently deeper
convection and re-ventilation over a period of approximately 1500
years. After the re-ventilation of the various sub-ba-sins during
the middle and late Holocene, deep-water renewal was more or less
similar to recent rates (Schmiedl et al. 2010b). Several species of
deep-water ostracods that are still common in the western
Mediterranean became extinct in the eastern Mediterranean Basin at
the onset of early Holocene S1 sapropel deposition and the related
anoxia (Van Harten 1987). The deep-water ostracode Bythocypris
obtusata apparently survived the oxygen crisis in the eastern basin
itself. This suggests that full oxygen depletion may not have
affected the bottom of all deep sub-basins and supports a midwater
oxygen-minimum model for these sub-basins (Van Harten 1987;
Schmiedl et al. 2010b).
These paleoclimatic findings suggest that eastern Mediterranean
pelagic and benthic marine ecosys-tems are capable of abrupt
transitions in response to gradual forcing. This is crucial for the
projection of whether an increase in oceanic moisture availability
under current and future warming could trigger a sudden
intensification of monsoon rainfall further inland from today’s
core monsoon region (Schewe and Levermann 2017).
Response of marine ecosystems to past changes in
productivity
In the western Mediterranean, productivity has shown an overall
decreasing trend since the early Hol-ocene with a marked fall in
productivity after the 8.2 ky BP dry-cold event (Ciampo 2004;
Jiménez-Espejo et al. 2007; Melki et al. 2009). Superimposed on
this long-term pattern, some studies show millennial–centennial
time scale variability linked with weakening and strengthening of
upwelling con-ditions that have been simultaneous to changes in
Western Mediterranean Deep Water (WMDW) for-mation in the Gulf of
Lions and by extent to the NAO over the past 7.7 ka (Ausín et al.
2015). These
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changes were accompanied by re-organization in coccolithophore
assemblages showing in particular, several high-amplitude
oscillations of the productivity indicator species F. profunda
(Ausín et al. 2015).
In the eastern Mediterranean, several proxy data support overall
increased productivity during Sapro-pel S1 in a high-nutrient
stratified environment (Gennari et al. 2009; Castañeda et al. 2010;
Mojtahid et al. 2015). This period is characterized by the highest
accumulation rates of planktonic foraminifera together with the
productivity indicator coccolithophore species F. profunda
(Incarbona et al. 2011; Mojtahid et al. 2015). After Sapropel 1, a
progressive decrease in surface water productivity was rec-orded
and surface and deep-sea ecosystems were driven by short-term
changes in food quantity and quality as well as in seasonality, all
of which are linked to millennial-scale changes in river runoff and
associated nutrient input (Kuhnt et al. 2008; Schmiedl et al.
2010b). Particularly, the last 2.9 ka encom-passed a succession of
three ecosystem states characterized by nutrient-limiting surface
waters from 2.9 to 1.1 ka, and during the Little Ice Age, and by
nutrient-rich waters from 1.1 to 0.54 ka (Medieval Climate anomaly)
(Mojtahid et al. 2015). These conditions were linked to periods of
low and high Nile River runoff respectively, in line with arid and
humid climate conditions in the Levant and Nile head-waters.
These findings imply that surface productivity in the overall
oligotrophic Mediterranean Sea responds rapidly to short and
long-term changes in nutrient input, either via rivers, winds or
upwelling activity, modifying the benthic-pelagic ecosystems by
extending into the entire food chain (Marino and Ziveri 2013),
ultimately increasing eutrophication.
Response of marine ecosystems to past changes in pH
Holocene reconstructions of paleo-pH have yet to be undertaken
in the Mediterranean. There is a promising raw data record of
planktonic foraminiferal (Neogloboquadrina incompta) δ11B and B/Ca.
These geochemical proxies can be used for paleo-pH and show an
overall decreasing trend in both sub-basins of the Mediterranean
Sea during the last deglacial episode of glacial-interglacial CO2
rise (Grelaud et al. 2012; Marino and Ziveri 2013). The response of
marine calcifiers to this trend can be estimated via planktonic
foraminifera shell weight that shows overall decreasing planktonic
calcifica-tion in response to this variability. In addition to this
general trend, periods of changing seawater car-bonate chemistry
can be observed, which could be linked to low/high primary
production activity such as the anomaly observed during Sapropel 1
period, which can be linked to enhanced mineralization of organic
matter.
These first studies show that Mediterranean marine calcifiers
responded to past changes in surface seawater carbonate chemistry
conditions. The extent to which this affects marine ecosystems
needs to be analyzed in the context of the current acidification in
the Mediterranean’s surface and deep seawaters.
4.1.2 Projected vulnerabilities and risks
4.1.2.1 Projected impacts and risks
As already discussed in Section 2.2.4.1, annual mean
temperatures in the Mediterranean are now 1.5°C above late 19th
century levels with magnitudes that vary locally depending on the
period of analysis, the region and the type of dataset. The diurnal
temperature range has also changed in some parts of the
Mediterranean (Section 2.2.4.1). In absolute terms, the warmest
parts are the southern and east-ern Mediterranean and the major
impact in these parts is the immigration of Indo-Pacific species
(around a thousand species), which has accelerated in recent years,
mainly for thermophilic species, due to rapid warming conditions
(more than 50% of Mediterranean non-indigenous species are in the
eastern Mediterranean) (Azzurro et al. 2011; Marbà et al. 2015;
Kletou et al. 2016; Bariche et al. 2017). All Mediterranean waters,
even the deepest, are affected by ocean acidification driven by
Mediterra-nean Sea uptake of atmospheric CO2 (Flecha et al. 2015;
Hassoun et al. 2015; Palmiéri et al. 2015; Ingrosso et al. 2017)
(Section 6.11). In addition, the effects of climate change are
amplified by other
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major non-climate-related anthropogenic forcings, as the
Mediterranean has one of the most popu-lated coastlines with a long
human history of exploitation of marine resources (with presently
one of the world’s most intense coastal and maritime tourism
areas), habitat degradation and plastic pollu-tion (Cózar et al.
2015; Compa et al. 2019). More information about sea use changes
and pollution are covered in Chapter 2.
The combination of various ongoing climate change processes
(e.g., sea warming, ocean acidification, and sea level rise;
Section 2.6) has caused detectable effects on marine organisms at
individual, popu-lation, and ecosystem scales (Fig. 4.4). Future
risks of seal level rise, marine heat waves, and ocean
acidification are also highlighted in Sections 6.9, 6.10 and 6.11
respectively. In fact, sponges, gorgoni-ans, bryozoans, molluscs,
and seagrasses are all affected by these drivers (Cerrano et al.
2006; Garra-bou et al. 2009; Bensoussan et al. 2010; Marba and
Duarte 2010), but primary producers, mainly cal-cifiers such as
coccolithophores, are among the most vulnerable organisms (Meier et
al. 2014). The impacts are expected to affect endemic and iconic
ecosystems including major reorganizations of the biota
distribution, species loss, marine productivity, increases in
non-indigenous species, and potential species extinction (Malcolm
et al. 2006; Ramírez et al. 2018; Gao et al. 2020).
Projected impacts on microbes
Sea warming may have effects on the virulence of pathogens
(viruses, parasites, etc.), favoring the frequency of
epidemiological events, as most pathogens are temperature sensitive
(Vezzulli et al. 2013) (see Section 4.1.1 and Section 2.3.4 in
Chapter 2 for more information about biological pollu-tants), as
observed for Vibrio shiloi, responsible for the whitening of the
coral Oculina patagonica in the eastern Mediterranean (Kushmaro et
al. 1998). This warming is also responsible for the expansion of
harmful and/or toxic microalgae, mainly dinobionts such as
Ostreopsis ovata, which produces palyt-oxins, a serious public
health hazard (Accoroni et al. 2016; Vila et al. 2016). Temperature
anomalies also seem to negatively affect the chemical defenses of
marine organisms (Thomas et al. 2007), allow-ing pathogens to act
undisturbed. Given the predicted rise in temperatures over the
coming decades, a better understanding of the factors and
mechanisms that affect the disease process will be of critical
importance in predicting future threats to temperate gorgonians
communities (Bally and Garrabou 2007), and other affected species
in the Mediterranean Sea.
In deep waters, a recent study has shown that deep-sea benthic
Archaea can be more sensitive to temperature shifts than their
bacterial counterparts. Changes in deep-water temperature may thus
alter the relative importance of Archaea in benthic ecosystem
processes (Danovaro et al. 2016). With rising deep-water
temperatures, the predicted positive response of prokaryotic
metabolism to tem-perature increases may accelerate oxygen
depletion in deep Mediterranean waters, with domino ef-fects on
carbon cycling and biogeochemical processes across the entire deep
basin (Luna et al. 2012). Along canyon-cut margins (e.g., the
western Mediterranean), warming may additionally reduce
den-sity-driven domino effects, leading to decreased organic matter
transport to the seafloor (Canals et al. 2006), though this very
process is also likely to reduce physical disturbance on the
seafloor and there-fore affect deep-sea ecosystems.
Projected impacts on primary and secondary production
Climate change affects the functioning of the biological
components of ecosystems, from the basis of the food webs
(plankton) to the higher trophic levels (e.g., predator fish).
Phytoplankton constitutes the autotrophic primary producers in the
pelagic food chains in marine waters and their annual cycle is
affected by many physical features that in turn control nutrient
levels. These include large horizontal gradients in temperature
(Izrael 1991). Due to their rapid turnover and fast responses to
environmen-tal changes, plankton is considered a suitable proxy to
highlight either environmental changes circum-scribed in space
and/or time or wider climatic variations. Warming, for example, is
responsible for the expansion of harmful and/or toxic microalgae,
mainly the dinobionts such as Ostreopsis ovata, which produces
palytoxins, a serious public health hazard (Accoroni et al. 2016;
Vila et al. 2016). A new study
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in the Eastern Mediterranean has shown the occurence of
important concentrations of biotoxins (do-moic acid, gymnodimines
and spirolides) in various marine organisms sampled from the
Lebanese shores (Hassoun et al. 2021). These concentrations were
correlated with the abundance of biotoxins' producers such as
Pseudo-nitzschia, Prorocentrum, Alexandrium, and other species that
could be oc-curring more frequently due to climate change (Hassoun
et al. 2021).
Moreover, phytoplankton species responsible for bloom at late
winter and at the beginning of spring (like Skeletonema costatum,
Nitzschia spp, Leptocylindrus danicus and L. minimus and others)
could start earlier, because features of temperate marine
planktonic ecosystems are not only sensitive to annual variations
in weather, but also any trends that might result from greenhouse
warming or other factors that affect the climate system and both
the density and timing of spring blooms will be altered in some
regions (Townsend et al. 1994).
The taxonomic compositions of phyto- and zooplankton may change
under the influence of changes in ocean structure (Kawasaki 1991;
Berline et al. 2012; Howes et al. 2015) (Section 2.2.7). A
thermo-philic phytoplankton species could proliferate especially in
some enriched areas and could be ichthyo-toxic or even toxic for
humans (Abboud-Abi Saab 2008, 2009; Accoroni et al. 2016;
Abboud-Abi Saab and Hassoun 2017). Some examples can explain such
variations. In the Mediterranean Sea, phyto-plankton biomass
abundance and sea surface thermal stratification show a strong
inverse relationship at seasonal and sub-basin scales. At
inter-annual and sub-basin scales, a gradual decline of the
phyto-plankton biomass across the entire central Mediterranean
occurs with a delay of one year (Volpe et al. 2012). In the
Adriatic Sea, during the past decade, the community structure and
seasonality of phyto-plankton have changed significantly. The
phytoplankton annual cycle has become more irregular with sudden
diatom blooms, reflecting the variability of meteorological events
in recent years (Totti et al. 2019).
Only a few regional studies have investigated the sensitivity of
the oligotrophic Mediterranean Sea to future climate change. The
first investigations considered only the changes in circulation.
For instance, a regional model of the northwestern Mediterranean
domain found that the effect of local stratifica-tion due to
climate change would have no drastic effect on the pelagic
ecosystem (Herrmann et al. 2014). However, one study investigated
the overall effects of a moderate climate change scenario (A1B
SRES) on Mediterranean biological productivity and plankton
communities and found an overall de-crease in phytoplankton biomass
in response to the stratification simulated in their dynamic
climate change scenario (Lazzari et al. 2014). A simulation was
carried out for an increase in integrated primary productivity
across the eastern Mediterranean Basin as a result of changes in
density (decreased strat-ification) (Macías et al. 2015). However,
conclusions from these studies remain limited by the fact that they
are based on non-transient simulations and present-day nutrient
inputs.
A new study has investigated the influence of both changes in
circulation and biogeochemical forcings (rivers and input at
Gib